Induced responses to above-ground and below-ground herbivores may interact via systemic signalling in plants. We investigated whether the impact of above-ground herbivory on root-knot nematode-induced responses depends on the nematode’s life cycle stages. Tomato plants were infected with the nematode (Meloidogyne incognita) for 5, 15 or 30 days before receiving Spodoptera exigua caterpillars above-ground. We collected root materials after 24 h of caterpillar feeding. We investigated phytohormones and α-tomatine levels, and the expression of defence and glycoalkaloid metabolism (GAME) marker genes in tomato roots. Nematode infection alone increased the endogenous root levels of jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), α-tomatine and the expression of the GLYCOALKALOID METABOLISM 1 (GAME1) gene mostly at 30 days post-nematode inoculation. Caterpillar feeding alone upregulated Lipoxygenase D and downregulated Basic-β-1-glucanase and GAME1 expression in roots. On nematode-infected plants, caterpillar feeding decreased JA levels, but it increased the expression of Leucine aminopeptidase A. The induction patterns of ABA and SA suggest that caterpillars cause cross-talk between the JA-signalling pathway and the SA and ABA pathways. Our results show that caterpillar feeding attenuated the induction of the JA pathway triggered by nematodes, mostly in the nematodes’ reproduction stage. These results generate a better understanding of the molecular and chemical mechanisms underlying frequent nematode–plant–caterpillar interactions in natural and agricultural ecosystems.

中文翻译：

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甜菜夜蛾草食性对南方根结线虫诱导的根反应的影响取决于线虫的生命周期阶段。

对地上和地下食草动物的诱导反应可能通过植物中的系统信号相互作用。我们研究了地上食草对根结线虫引起的反应的影响是否取决于线虫的生命周期阶段。番茄植株被线虫（Meloidogyne incognita）感染5、15或30天，然后在地上接受甜菜夜蛾毛虫。毛毛虫取食24小时后收集根部材料。我们研究了番茄根中植物激素和 α-番茄碱的水平，以及防御和配糖生物碱代谢 (GAME) 标记基因的表达。仅线虫感染增加了茉莉酸 (JA)、水杨酸 (SA)、脱落酸 (ABA)、α-番茄碱的内源根水平以及糖碱代谢 1 (GAME1)基因的表达，主要发生在线虫接种后 30 天。单独喂食毛毛虫会上调根中脂氧合酶 D 的表达并下调碱性-β-1-葡聚糖酶和GAME1 的表达。在线虫感染的植物上，毛虫取食降低了 JA 水平，但增加了亮氨酸氨肽酶 A的表达。ABA 和 SA 的诱导模式表明毛虫会引起 JA 信号通路与 SA 和 ABA 通路之间的串扰。我们的结果表明，毛毛虫取食减弱了线虫触发的 JA 途径的诱导，主要是在线虫的繁殖阶段。这些结果使人们更好地了解自然和农业生态系统中线虫-植物-毛毛虫频繁相互作用的分子和化学机制。